Top

Published in:

Open Access 01-09-2014 | Original Article

Cognitive subtypes of dyslexia are characterized by distinct patterns of grey matter volume

Authors: Katarzyna Jednoróg, Natalia Gawron, Artur Marchewka, Stefan Heim, Anna Grabowska

Published in: Brain Structure and Function | Issue 5/2014

Abstract

The variety of different causal theories together with inconsistencies about the anatomical brain markers emphasize the heterogeneity of developmental dyslexia. Attempts were made to test on a behavioral level the existence of subtypes of dyslexia showing distinguishable cognitive deficits. Importantly, no research was directly devoted to the investigation of structural brain correlates of these subtypes. Here, for the first time, we applied voxel-based morphometry (VBM) to study grey matter volume (GMV) differences in a relatively large sample (n = 46) of dyslexic children split into three subtypes based on the cognitive deficits: phonological, rapid naming, magnocellular/dorsal, and auditory attention shifting. VBM revealed GMV clusters specific for each studied group including areas of left inferior frontal gyrus, cerebellum, right putamen, and bilateral parietal cortex. In addition, using discriminant analysis on these clusters 79 % of cross-validated cases were correctly re-classified into four groups (controls vs. three subtypes). Current results indicate that dyslexia may result from distinct cognitive impairments characterized by distinguishable anatomical markers.

Available only for authorised users

Amico F, Stauber J, Koutsouleris N, Frodl T (2011) Anterior cingulate cortex gray matter abnormalities in adults with attention deficit hyperactivity disorder: a voxel-based morphometry study. Psychiatry Res 191:31–35PubMedCrossRef

Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113PubMedCrossRef

Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839–851PubMedCrossRef

Behrmann M, Geng JJ, Shomstein S (2004) Parietal cortex and attention. Curr Opin Neurobiol 14:212–217PubMedCrossRef

Bogdanowicz M, Jaworowska A, Krasowicz-Kupis G, Matczak A, Pelc-Pękala O, Pietras I, Stańczak J, Szczerbiński M (2008) Diagnoza dysleksji u uczniów klasy III szkoły podstawowej. Pracownia Testów Psychologicznych, Warszawa

Bosse ML, Tainturier MJ, Valdois S (2007) Developmental dyslexia: the visual attention span deficit hypothesis. Cognition 104:198–230PubMedCrossRef

Brambati SM, Termine C, Ruffino M, Stella G, Fazio F, Cappa SF, Perani D (2004) Regional reductions of gray matter volume in familial dyslexia. Neurology 63:742–745PubMedCrossRef

Brett M, Anton J-C, Valabregue R, Poline J-B (2002) Region of interest analysis using an SPM toolbox (abstract). Presented at the 8th international conference on functional mapping of the human brain, Sendai, 2–6 June 2002

Brown WE, Eliez S, Menon V, Rumsey JM, White CD, Reiss AL (2001) Preliminary evidence of widespread morphological variations of the brain in dyslexia. Neurology 56:781–783PubMedCrossRef

Bryden DW, Johnson EE, Tobia SC, Kashtelyan V, Roesch MR (2011) Attention for learning signals in anterior cingulate cortex. J Neurosci 31:18266–18274PubMedCentralPubMedCrossRef

Eckert MA, Leonard CM, Wilke M, Eckert M, Richards T, Richards A, Berninger V (2005) Anatomical signatures of dyslexia in children: unique information from manual and voxel based morphometry brain measures. Cortex 41:304–315PubMedCrossRef

Eden GF, Zeffiro TA (1998) Neural systems affected in developmental dyslexia revealed by functional neuroimaging. Neuron 21:279–282PubMedCrossRef

Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 22:676–687PubMedCrossRef

Heim S, Grande M (2012) Fingerprints of developmental dyslexia. Trends Neurosci Educ 1:10–14CrossRef

Heim S, Tschierse J, Amunts K, Wilms M, Vossel S, Willmes K, Grabowska A, Huber W (2008) Cognitive subtypes of dyslexia. Acta Neurobiol Exp 68:73–82

Heim S, Grande M, Pape-Neumann J, van Ermingen M, Meffert E, Grabowska A, Huber W, Amunts K (2010a) Interaction of phonological awareness and ‘magnocellular’ processing during normal and dyslexic reading: behavioural and fMRI investigations. Dyslexia 16:258–282PubMedCrossRef

Heim S, Grande M, Meffert E, Eickhoff SB, Schreiber H, Kukolja J, Shah NJ, Huber W, Amunts K (2010b) Cognitive levels of performance account for hemispheric lateralisation effects in dyslexic and normally reading children. Neuroimage 53:1346–1358PubMedCrossRef

Heilman KM, Voeller K, Alexander AW (1996) Developmental dyslexia: a motor-articulatory feedback hypothesis. Ann Neurol 39:407–412PubMedCrossRef

Hernandez AE, Fiebach CJ (2006) The brain bases of reading late learned words: evidence from functional MRI. Vis Cogn 13:1027–1043CrossRef

Hoeft F, Meyler A, Hernandez A, Juel C, Taylor-Hill H, Martindale JL, McMillon G, Kolchugina G, Black JM, Faizi A, Deutsch GK, Siok WT, Reiss AL, Whitfield-Gabrieli S, Gabrieli JD (2007) Functional and morphometric brain dissociation between dyslexia and reading ability. Proc Natl Acad Sci USA 104:4234–4239PubMedCentralPubMedCrossRef

Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3:284–291PubMedCrossRef

Joly O, Ramus F, Pressnitzer D, Vanduffel W, Orban GA (2012) Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys. Cereb Cortex 22:838–853PubMedCrossRef

Kibby MY, Fancher JB, Markanen R, Hynd GW (2008) A quantitative magnetic resonance imaging analysis of the cerebellar deficit hypothesis of dyslexia. J Child Neurol 23:368–380PubMedCentralPubMedCrossRef

Kronbichler M, Wimmer H, Staffen W, Hutzler F, Mair A, Ladurner G (2008) Developmental dyslexia: gray matter abnormalities in the occipitotemporal cortex. Hum Brain Mapp 29:613–625PubMedCrossRef

Lallier M, Thierry G, Tainturier MJ, Donnadieu S, Peyrin C, Billard C, Valdois S (2009) Auditory and visual stream segregation in children and adults: an assessment of the amodality assumption of the ‘sluggish attentional shifting’ theory of dyslexia. Brain Res 1302:132–147PubMedCrossRef

Liu T, Fuller S, Carrasco M (2006) Attention alters the appearance of motion coherence. Psychon Bull Rev 13:1091–1096PubMedCrossRef

Murtha S, Chertkow H, Beauregard M, Dixon R, Evans A (1996) Anticipation causes increased blood flow to the anterior cingulate cortex. Hum Brain Mapp 4:103–112PubMedCrossRef

Nicolson RI, Fawcett AJ, Dean P (2001) Developmental dyslexia: the cerebellar deficit hypothesis. Trends Neurosci 24:508–511PubMedCrossRef

Pernet C, Andersson J, Paulesu E, Demonet JF (2009) When all hypotheses are right: a multifocal account of dyslexia. Hum Brain Mapp 30:2278–2292PubMedCrossRef

Ramus F, Ahissar M (2012) Developmental dyslexia: The difficulties of interpreting poor performance, and the importance of normal performance. Cogn Neuropsychol

Ramus F, Rosen S, Dakin SC, Day BL, Castellote JM, White S, Frith U (2003) Theories of developmental dyslexia: insights from a multiple case study of dyslexic adults. Brain 126:841–865PubMedCrossRef

Richardson FM, Price CJ (2009) Structural MRI studies of language function in the undamaged brain. Brain Struct Funct 213:511–523PubMedCentralPubMedCrossRef

Seidman LJ, Valera EM, Makris N, Monuteaux MC, Boriel DL, Kelkar K, Kennedy DN, Caviness VS, Bush G, Aleardi M, Faraone SV, Biederman J (2006) Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biol Psychiatry 60:1071–1080PubMedCrossRef

Seidman LJ, Biederman J, Liang L, Valera EM, Monuteaux MC, Brown A, Kaiser J, Spencer T, Faraone SV, Makris N (2011) Gray matter alterations in adults with attention-deficit/hyperactivity disorder identified by voxel based morphometry. Biol Psychiatry 69:857–866PubMedCentralPubMedCrossRef

Silani G, Frith U, Demonet JF, Fazio F, Perani D, Price C, Frith CD, Paulesu E (2005) Brain abnormalities underlying altered activation in dyslexia: a voxel based morphometry study. Brain 128:2453–2461PubMedCrossRef

Steinbrink C, Vogt K, Kastrup A, Müller HP, Juengling FD, Kassubek J, Riecker A (2008) The contribution of white and gray matter differences to developmental dyslexia: insights from DTI and VBM at 3.0 T. Neuropsychologia 46:3170–3178PubMedCrossRef

Talcott JB, Hansen PC, Assoku EL, Stein JF (2000) Visual motion sensitivity in dyslexia: evidence for temporal and energy integration deficits. Neuropsychologia 38:935–943PubMedCrossRef

Tettamanti M, Moro A, Messa C, Moresco RM, Rizzo G, Carpinelli A, Matarrese M, Fazio F, Perani D (2005) Basal ganglia and language: phonology modulates dopaminergic release. NeuroReport 16:397–401PubMedCrossRef

Turkeltaub PE, Gareau L, Flowers DL, Zeffiro TA, Eden GF (2003) Development of neural mechanisms for reading. Nat Neurosci 6:767–773PubMedCrossRef

Uncapher MR, Rugg MD (2009) Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information. J Neurosci 29:8270–8279PubMedCentralPubMedCrossRef

Vinckenbosch E, Robichon F, Eliez S (2005) Gray matter alteration in dyslexia: converging evidence from volumetric and voxel-by-voxel MRI analyses. Neuropsychologia 43:324–331PubMedCrossRef

Weissman DH, Mangun GR, Woldorff MG (2002) A role for top-down attentional orienting during interference between global and local aspects of hierarchical stimuli. Neuroimage 17:1266–1276PubMedCrossRef

Weissman DH, Gopalakrishnan A, Hazlett CJ, Woldorff MG (2005) Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cereb Cortex 15:229–237PubMedCrossRef

White S, Milne E, Rosen S, Hansen P, Swettenham J, Frith U, Ramus F (2006) The role of sensorimotor impairments in dyslexia: a multiple case study of dyslexic children. Dev Sci 9:237–255PubMedCrossRef

Wilke M, Holland SK, Altaye M, Gaser C (2008) Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 41:903–913PubMedCrossRef

Wimmer H, Schurz M, Sturm D, Richlan F, Klackl J, Kronbichler M, Ladurner G (2010) A dual-route perspective on poor reading in a regular orthography: an fMRI study. Cortex 46:1284–1298PubMedCentralPubMedCrossRef

Wolf M, Bowers P (1999) The “double-deficit hypothesis” for the developmental dyslexias. J Educ Psychol 91:1–24CrossRef

Title: Cognitive subtypes of dyslexia are characterized by distinct patterns of grey matter volume
Authors: Katarzyna Jednoróg
Natalia Gawron
Artur Marchewka
Stefan Heim
Anna Grabowska
Publication date: 01-09-2014
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 5/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-013-0595-6

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Cognitive subtypes of dyslexia are characterized by distinct patterns of grey matter volume

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2014

Superior temporal metabolic changes related to auditory hallucinations: a 31P-MR spectroscopy study in antipsychotic-free schizophrenia patients

A role for anterior thalamic nuclei in contextual fear memory

Organization and chemical neuroanatomy of the African elephant (Loxodonta africana) hippocampus

Neural mechanisms of oxytocin receptor gene mediating anxiety-related temperament

Convergence of cortical and thalamic input to direct and indirect pathway medium spiny neurons in the striatum

Distribution of the glucocorticoid receptor in the human amygdala; changes in mood disorder patients